American Journal of Epidemiology Advance Access originally published online on March 10, 2007
American Journal of Epidemiology 2007 165(12):1405-1412; doi:10.1093/aje/kwm028
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
ORIGINAL CONTRIBUTIONS |
Growth Trajectory Matters: Interpreting the Associations among Birth Weight, Concurrent Body Size, and Systolic Blood Pressure in a Cohort Study of 378,707 Swedish Men
1 Department of Social Medicine, University of Bristol, Bristol, United Kingdom
2 Department of Epidemiology and Population Health, London School of Hygiene and Tropical Medicine, London, United Kingdom
3 Department of Public Health Sciences, Karolinska Institute, Stockholm, Sweden
4 Division of Epidemiology, Stockholm Center of Public Health, Stockholm, Sweden
Correspondence to Dr. Finn Rasmussen, Child and Adolescent Public Health Epidemiology Group, Department of Public Health Sciences, Karolinska Institute, Norrbacka Building, SE-171 76 Stockholm, Sweden (e-mail: finn.rasmussen{at}ki.se).
Received for publication August 14, 2006. Accepted for publication December 5, 2006.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
The interpretation of the inverse association of birth weight with adult blood pressure after adjustment for concurrent size has been debated. In a large sample (n = 378,707) of Swedish men aged 18 years, born between 1973 and 1984, the authors found considerable variation in birth weight within strata of identical adult body mass index (to the nearest kg/m2; range: 17–33 kg/m2), weight (nearest kg; range: 52–100 kg), and height (nearest cm; range: 164–196 cm). The regression coefficient of systolic blood pressure on birth weight was inverse and the same within strata of identical body mass index (pinteraction = 0.80), weight (p = 0.79), and height (p = 0.35). When the analyses were restricted to those who were born between 39 and 41 weeks' gestation, consistent inverse associations remained within strata of identical adult size. Findings were similar when hypertension (rather than mean systolic blood pressure) was the outcome. These findings demonstrate that, for male babies who grow to be the same size at age 18 years, those who were of lower birth weight have on average higher blood pressure and a greater risk of hypertension. They suggest that growth between conception and early adulthood has relevance to understanding the etiology and, hence, prevention of high blood pressure.
adult; birth weight; blood pressure; body mass index; body weight; growth; hypertension; male
Abbreviations: CI, confidence interval; SD, standard deviation
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Several observers have questioned the appropriateness of adjusting for concurrent size when examining the association of birth weight with later systolic blood pressure (1–3). Others have questioned whether investigators correctly justify or interpret the adjusted results, rather than emphatically stating that adjustment is inappropriate (4–6). In the majority of studies that have examined the association of birth weight with systolic blood pressure, a weak inverse association has been found that becomes stronger upon adjustment for concurrent body size (1).
Tu et al. (3) suggest that adjustment for concurrent size when examining the association of birth weight with blood pressure risks committing a statistical fallacy—creating an association where none exits. In response, Cole asserts that the simulations of Tu et al. do not extend what can be demonstrated by simple algebra and that neither "help[s] to decide whether such an adjustment is valid" (5, p. 394). He suggests that a valid interpretation of these adjusted results is that weight change, rather than birth weight (or perinatal factors that influence birth weight), is the more important etiologic factor (4). This is actually consistent with the statement by Tu et al. that the correct interpretation of the birth weight-blood pressure association adjusted for concurrent size is that "if all babies grew to the same size in adulthood, lower-birth-weight babies would, on average, have higher blood pressure in adulthood"(3, p. 31). However, Tu et al. go on to report that "this conclusion is counterfactual since low-birth-weight babies will, on average, be smaller than heavy-birth-weight babies in adulthood" (3, p. 31). Although it is true that, on average, low-birth-weight babies will be smaller than heavy-birth-weight babies, it is also true that the birth weight-adult weight correlations are weak and, therefore, it is a fact that there will be a wide variation in birth weights among adults who are all the same size. We set out to demonstrate this with real data by examining the variation in birth weight within strata of men with the same adult body mass index (to 1 kg/m2), weight (to 1 kg), and height (to 1 cm) and to examine the association of birth weight with blood pressure within these strata. A prospective record linkage study of Swedish men provided us with the large numbers of participants necessary to be able to examine men in strata of the same adult sizes across the range of population level sizes.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
The study cohort consists of all men born in Sweden between 1973 and 1984, who were still alive and completed their medical examination for conscription purposes (n = 413,683). For individuals born between 1973 and 1984, the conscript medical examinations took place between 1991 and 2001. The date of birth of the index participant, together with the mother's age at birth and the parents' unique identity numbers, was extracted from the Swedish Multigeneration Register. A linkage was made between these data and the Swedish Medical Birth Register (providing data on birth weight, gestational age, maternal parity, maternal diagnoses during pregnancy, and mode of delivery), the Swedish military service conscription examination (data on age, height, weight, and systolic and diastolic blood pressure), and the Population and Housing Census of 1970, 1980, and 1990 (data on family socioeconomic position). These linkages were achieved by using the unique personal identification code assigned to each person living in Sweden and were carried out with the permission of the Ethics Committee of the Karolinska Institute, Stockholm.
The record linkage and details of the cohort have been described in detail previously (7).
We excluded multiple births, anyone with implausible values, and anyone with missing data on any variables used in this study (7). After these exclusions, the study population comprised 386,485 men (93 percent of eligible men). In order to examine the associations within strata of men with the same body mass index (to the nearest kg/m2), the same weight (to the nearest kg), and the same height (to the nearest cm) with reasonable precision, we decided a priori to include only the strata of identical body mass index, weight, or height in which there were at least 1,000 men. This resulted in excluding an additional 7,778 men who had a body mass index of less than 17 kg/m2 or greater than 33 kg/m2, weight less than 52 kg or greater than 100 kg, or height less than 164 cm or greater than 196 cm. With these exclusions 378,707 men (92 percent) remained in the analyses.
Data on birth weight were measured by midwives or physicians shortly after birth, and data on gestational age were abstracted from the obstetric notes. During the years covered by this study, the law required all Swedish males to attend the Swedish military service conscription examination, which usually takes place when they are aged 18 years. The only reasons accepted for not attending were foreign citizenship or a severe chronic medical condition or handicap. The conscription examination is a test of suitability for military service; thus, the medical records from the conscription examination include individuals who were subsequently exempted from military service. Height and weight were measured by use of standard procedures with the men in underclothes and without shoes. Blood pressure was measured on the first day of the induction examination after 5–10 minutes' rest in the supine position. If the systolic blood pressure was 145 mmHg or below and the diastolic blood pressure was between 50 and 85 mmHg, no further measurements were made. If the measurements were outside these limits, a second measurement was made on the next day. In this case, the result of the second measure was entered into the register. For diastolic blood pressure, there was evidence of digit preference (rounding of values) to the nearest 10 mmHg; this was less of a problem for systolic blood pressure, which tended to be rounded to the nearest 2 mmHg (7). We have therefore assessed only the associations with systolic blood pressure in the main analyses presented here. We also examined associations with hypertension (defined, according to the Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure (8), as systolic blood pressure >140 mmHg or diastolic blood pressure >90 mmHg).
Internally standardized birth-weight-for-gestational-age (per completed week between 35 and 44 weeks) z scores were derived. This allows for a measure of intrauterine growth. We present the distributions (mean and standard deviation or percent) of birth weight, systolic blood pressure, and hypertension in each group of men with the same body mass index, weight, and height. We used multivariable linear regression to estimate the association of birth weight with systolic blood pressure within strata of identical body mass index, weight, and height and multivariable logistic regression to assess the association of birth weight with hypertension, adjusting in both sets of analyses for examination center, age at conscription, year of conscription, and family socioeconomic position at birth and in adulthood (based on head of household occupation at birth and around the time of conscription) (7). A likelihood ratio test was used to compute a test for statistical interaction between birth weight and body mass index, weight, or height in their association with systolic blood pressure or hypertension (i.e., to test whether the association of birth weight with blood pressure/hypertension varied between the strata of men with identical body mass index, weight, or height). In order to strengthen the use of birth weight for gestational age as a measure of intrauterine growth, we repeated all of the analyses including only those with gestational ages between 39 and 41 weeks, which included 60 percent of our study sample. All analyses were undertaken in STATA, version 9.0, software (StataCorp LP, College Station, Texas).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Table 1 shows the characteristics of study participants. All of the men were aged between 17 and 20 years when their blood pressure, weight, and height were measured. Birth weight was only weakly positively correlated with body mass index at mean age 18 years and was modestly associated with weight and height at age 18; adult body mass index and weight were strongly positively correlated with each other, whereas adult height was only weakly correlated with body mass index (table 2). Birth weight had a weak inverse correlation with systolic blood pressure, and height, weight, and body mass index were positively correlated with systolic blood pressure.
|
|
Table 3 shows the variation in birth weight, systolic blood pressure, and hypertension in strata of men defined by having the same body mass index. Although it is clear that mean birth weight increases across the groups as body mass index increases, there are also considerable variation of birth weight within each group of men who have the same adult body mass index and considerable overlap in the 5th–95th percentile range of birth weights across all strata. Thus, the range of birth weights that includes 90 percent of the men with the lowest body mass index in this sample is very similar to the range of birth weights including 90 percent of the men with the highest body mass index. These findings are consistent with the weak correlation between birth weight and adult body mass index. The mean systolic blood pressure and percentage with hypertension increased as body mass index increased. When we undertook similar analyses within strata of men with identical adult weight, we also found considerable variation of birth weights within each stratum and considerable overlap in birth weight ranges between different groups defined by identical adult weight (full data not shown). For strata of identical adult height, the findings were similar to those for body mass index and weight (table 4).
|
|
The association of birth weight with systolic blood pressure was the same in each stratum of men with the same body mass index (figure 1; pinteraction = 0.80). There was also a consistent inverse association of birth weight with systolic blood pressure across strata of identical adult weight (figure 2; pinteraction = 0.79) and strata of identical adult height (figure 3; pinteraction = 0.35). When adjustment was made for age, year of conscription, examination center, and family socioeconomic position, a one-unit greater birth-weight-for-gestational-age z score (equivalent to 1 standard deviation (SD) of birth weight, where 1 SD = 503.6 g) was associated with a 0.17-mmHg lower blood pressure measurement (regression coefficient: –0.17 mmHg, 95 percent confidence interval (CI): –0.20, –0.13). Additional adjustment for parity and maternal experience of pregnancy-induced hypertension did not alter these associations. With additional adjustment for body mass index (to the age, year of conscription, examination center, and family socioeconomic position adjusted model), the regression coefficient increased to –0.31 mmHg (95 percent CI: –0.35, –0.28). Similarly, additional adjustment for weight to the confounder-adjusted model resulted in an increase of the coefficient to –0.63 mmHg (95 percent CI: –067, –0.58), as did additional adjustment for height, which resulted in an increase to –0.45 mmHg (95 percent CI: –0.49, –0.42). Note that each of these coefficients is adjusted for only one of the adult measures of size (either body mass index, weight, or height) in addition to the standard covariates included in all models as potential confounding factors. The resulting coefficients after adjustment for each measure of adult size are consistent with the effect estimates within the strata of men with identical body mass index, weight, or height, as shown in figures 1–3.
|
|
|
There was also a consistent inverse association of birth weight with hypertension in all strata of men with identical body mass index (full data not shown; pinteraction = 0.93), identical weight (full data not shown; pinteraction = 0.84), and identical height (full data not shown; pinteraction = 0.68). The adjusted (age, year of conscription, examination center, family socioeconomic position) odds ratio of hypertension for each 1-SD increase in birth weight was 0.96 (95 percent CI: 0.95, 0.97). Further adjustment for body mass index strengthened this to 0.94 (95 percent CI: 0.93, 0.95), adjustment for weight strengthened it to 0.90 (95 percent CI: 0.89, 0.91), and adjustment for height strengthened it to 0.92 (95 percent CI: 0.91, 0.93).
In linear regression models adjusted for age, year of conscription, examination center, family socioeconomic position, and birth weight, a 1-SD greater adult body mass index (1 SD = 2.9 kg/m2) was associated with a 1.85-mmHg greater systolic blood pressure measurement (95 percent CI: 1.82, 1.89), a 1-SD greater adult weight (1 SD = 11.5 kg) was associated with a 2.01-mmHg greater blood pressure measurement (95 percent CI: 1.96, 2.06), and a 1-SD greater adult height (1 SD = 6.2 cm) was associated with a 1.11-mmHg greater blood pressure measurement (95 percent CI: 1.07, 1.45). The adjusted (age, year of conscription, examination center, family socioeconomic position, and birth weight) odds ratio of hypertension for a 1-SD greater adult body mass index was 1.34 (95 percent CI: 1.33, 1.35), for a 1-SD greater adult weight was 1.38 (95 percent CI: 1.37, 1.39), and for a 1-SD greater adult height was 1.18 (95 percent CI: 1.17, 1.19). Additional adjustment for parity and maternal experience of pregnancy-induced hypertension did not alter these associations.
When all of the analyses were repeated, with restriction to men with gestational ages of 39–41 weeks, the findings were essentially the same as those presented here.
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
We have demonstrated that, within extremely narrowly defined strata of body mass index, weight, and height at age 18 years, there are considerable variation in birth weight and a consistent inverse association of birth weight with systolic blood pressure. The interpretation of these findings is that, among male babies who grow to the same size at age 18, those who were of lower birth weight have, on average, higher blood pressure and greater risk of hypertension. Contrary to the conclusions reached by some others (1, 3), we believe that these observations provide etiologic insights and that they identify individuals at risk of higher blood pressure, an established risk factor for cardiovascular disease (9, 10).
Our findings are consistent with the simulations of Tu et al. (3). The wide range of birth weights within strata of adult size are what one would expect as a result of the relatively weak correlations between birth size and later adult size. Our work adds to that of Tu et al. by demonstrating, with real data, the extent of variation in birth weight in adults with identical size. By asserting that the correct interpretation of the adjusted (for concurrent size) association is counterfactual, Tu et al. imply that it is implausible for low-birth-weight individuals to have greater adult size than higher-birth-weight individuals (3). Our data demonstrate that, although on average those of lower birth weight have lower adult size, within each stratum of individuals with identical adult size there are considerable variation of birth weight and overlap between groups of identical size. As such, in real life a large proportion of individuals have low birth weight and a large adult size and vice versa. One possible interpretation of the counterfactual argument is that it is implausible to imagine an intervention or biologic process that results in lower birth weight and does not also directly result in lower adult size. In reality, there are a number of processes that counter this argument. One of the strongest determinants of poor intrauterine growth and, hence, low birth weight is maternal smoking during pregnancy (11). However, a number of studies that have examined the association between maternal smoking during pregnancy and later body mass index in offspring find that it is associated with greater body mass index (12, 13), rather than lower body mass index, as would be expected from the counterfactual argument invoked by Tu et al. (3). Similarly, twins have lower birth weight than singletons, but adult size does not differ between twins and nontwins.
We agree with Cole (5), who points out that neither simulations nor algebra can determine whether adjustment for concurrent size (or any other variables) invalidates causal inference of this (or any other) association. What is important is that investigators justify why they have adjusted for concurrent size in examining the association of birth weight with blood pressure (or other adult outcomes) and that, after adjustment, their results are correctly interpreted (3, 5, 6). Of particular relevance to the developmental origins hypothesis, neither the unadjusted nor the adjusted (for concurrent size) association can confirm an intrauterine effect on blood pressure (4, 5). One way to interpret our results, as well as those of others who have controlled for concurrent size, is to say that the growth trajectory between conception and adulthood influences the mean blood pressure and risk of hypertension. The basis for this statement is that, if gestational age is taken into account, birth weight reflects intrauterine growth; thus, those with lower birth weight for gestational age have had slower intrauterine growth. We have taken gestational age into account here by standardizing birth weight for gestational age in our main analyses and also by demonstrating that our findings are not changed when we include only men who were born at the same gestational age (within a 3-week period of 39–41 weeks). The inverse association of systolic blood pressure with birth weight standardized for gestational age within men of the same size in adulthood suggests that trajectories of below average intrauterine growth (as discussed above: those with lower birth weight for gestational age have slower intrauterine growth) and/or increased growth postnatally (by definition, once we hold adult size constant as we do here, those who were smaller at birth must have grown more rapidly, on average, than those who were larger at birth to reach this same adult size) have an adverse effect upon adult blood pressure.
How might these growth trajectories between conception and adulthood affect blood pressure? It is possible that, among a group of individuals with the same adult size, the growth trajectory associated with being relatively small at birth may produce a more adipose adult body composition than among those who are larger at birth. It may be that it is this level of adiposity that is detrimental to blood pressure and cardiovascular health in general. The finding that birth weight was more strongly positively associated with lean mass than fat mass in a study of 143 older people (14), while requiring further replication, supports this suggestion. There is increasing evidence that intrauterine growth retardation results, at least in part, from maternal endothelial dysfunction and that, in mothers, the combination of this endothelial dysfunction with greater adiposity and metabolic abnormalities results in gestational hypertension or preeclampsia (15). It is conceivable that shared familial environmental and genetic factors link maternal endothelial dysfunction to similar pathology in their offspring, and that this explains the association of lower birth weight with higher blood pressure. The combination of this inherited endothelial dysfunction and greater adiposity in adulthood may (as in the mothers who develop preeclampsia) (15) be particularly detrimental. We do not have measures of fat and lean mass in our sample or of maternal and offspring endothelial function in order to test these hypotheses further.
The main strength of this study is its very large size, which enables us to examine associations of birth weight with blood pressure within groups of individuals of the same adult body mass index, weight, and height with good levels of precision. The range of body mass index (17–33 kg/m2), weight (52–100 kg), and height (164–196 cm) that we were able to examine covers the range seen among young men in most high-income countries. Measurement error, in particular, in the assessment of systolic blood pressure, is likely to be larger than in studies that use standardized research protocols (rather than routine army medical data), and this may mean that some of our results are underestimations of the true effects (7). Finally, our study is of men within a very narrow age range (the vast majority being 18 years), and so these results are not necessarily generalizable to women and individuals of older age.
The inverse association of birth weight with systolic blood pressure was weak, both with and without adjustment for concurrent size, and the public health importance of such weak associations has been questioned (16). Two considerations are important here. First, birth weight per se is unlikely to be the causal factor with respect to greater blood pressure or other adult outcomes. Rather, it is a proxy for intrauterine or postnatal exposures, such as maternal cardiovascular health, placentation, fetal nutrition, postnatal nutrition, and genotype, that influence growth trajectory and later adult disease. Further, research needs to determine which of these possibilities is most important in explaining the associations that we have found. Second, there is evidence that the association of birth weight with later blood pressure increases with increasing age at which blood pressure is assessed (17). In a recent study, the simple sex-adjusted association of birth weight with systolic blood pressure in those aged less than 25 years at the time of systolic blood pressure assessment (equivalent to our population) was –0.08 (95 percent CI: –1.3, 1.1) mmHg per 1 kg of birth weight, whereas in those who had their blood pressure assessed at age 55 years or more, it was –3.9 (95 percent CI: –6.7, –1.1) mmHg (17). Thus, the associations that we present here, with blood pressure assessed at a mean age of 18 years, may become stronger as this cohort ages.
To conclude, we agree that care is required to correctly interpret "adjusted" regression coefficients in any epidemiologic study. Our findings illustrate that, among babies who grow to be the same size at age 18 years, those who were of lower birth weight for gestational age (and hence had slower intrauterine growth rates) have, on average, higher blood pressure. Hence, growth trajectory from conception to adulthood matters. Understanding the biologic mechanisms that underlie the association of trajectory with later blood pressure and cardiovascular disease is important. If the combination of lower birth weight and greater size in later life is causally related to higher blood pressure and poorer cardiovascular health, this will have particularly detrimental effects in developing countries currently undergoing rapid urbanization and shifts to Western diets and lifestyles (18).
|
ACKNOWLEDGMENTS |
|---|
Conflict of interest: none declared.
|
References |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
- Huxley R, Neil A, Collins R. Unravelling the "fetal origins" hypothesis: is there really an inverse association between birth weight and future blood pressure? Lancet (2002) 360:659–65.[CrossRef][Web of Science][Medline]
- Hernan MA, Hernandez-Diaz S, Werler MM, et al. Causal knowledge as a prerequisite for confounding evaluation: an application to birth defects epidemiology. Am J Epidemiol (2002) 155:176–84.
[Abstract/Free Full Text] - Tu YK, West R, Ellison GT, et al. Why evidence for the fetal origins of adult disease might be a statistical artifact: the "reversal paradox" for the relation between birth weight and blood pressure in later life. Am J Epidemiol (2005) 161:27–32.
[Abstract/Free Full Text] - Lucas A, Fewtrell MS, Cole TJ. Fetal origins of adult disease—the hypothesis revisited. BMJ (1999) 319:245–9.
[Free Full Text] - Cole TJ. Re: "Why evidence for the fetal origins of adult disease might be a statistical artifact: the ‘reversal paradox’ for the relation between birth weight and blood pressure in later life." (Letter). Am J Epidemiol (2006) 162:394–5.[CrossRef][Web of Science]
- Weinberg CR. Invited commentary: Barker meets Simpson. Am J Epidemiol (2005) 161:33–5.
[Free Full Text] - Leon DA, Johansson M, Rasmussen F. Gestational age and growth rate of fetal mass are inversely associated with systolic blood pressure in young adults: an epidemiologic study of 165,136 Swedish men aged 18 years. Am J Epidemiol (2000) 152:597–604.
[Abstract/Free Full Text] - Chobanian AV, Bakris GL, Black HR, et al. The Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure: the JNC 7 report. JAMA (2003) 289:2560–72.
[Abstract/Free Full Text] - Lawes CM, Bennett DA, Parag V, et al. Blood pressure indices and cardiovascular disease in the Asia Pacific region: a pooled analysis. Hypertension (2003) 42:69–75.
[Abstract/Free Full Text] - Blood Pressure Lowering Treatment Trialists' Collaboration. Effects of different blood-pressure-lowering regimens on major cardiovascular events: results of prospectively-designed overviews of randomised trials. Lancet (2003) 362:1527–35.[CrossRef][Web of Science][Medline]
- Kramer MS. Determinants of low birth weight: methodological assessment and meta-analysis. Bull World Health Organ (1987) 65:663–737.[Web of Science][Medline]
- Power C, Jefferis BJ. Fetal environment and subsequent obesity: a study of maternal smoking. Int J Epidemiol (2002) 31:413–19.
[Abstract/Free Full Text] - Al Mamun A, Lawlor DA, Alati R, et al. Does maternal smoking during pregnancy have a direct effect on future offspring obesity? Evidence from a prospective birth cohort study. Am J Epidemiol (2006) 164:317–25.
[Abstract/Free Full Text] - Gale CR, Martyn CN, Kellingray S, et al. Intrauterine programming of adult body composition. J Clin Endocrinol Metab (2001) 86:267–72.
[Abstract/Free Full Text] - Ness RB, Sibai BM. Shared and disparate components of the pathophysiologies of fetal growth restriction and preeclampsia. Am J Obstet Gynecol (2006) 195:40–9.[Web of Science][Medline]
- Whincup PH, Cook DG, Geleijnse JM. A life course approach to blood pressure. In: A life course approach to chronic disease epidemiology—Kuh D, Ben-Shlomo Y, eds. (2004) 2nd ed. Oxford, United Kingdom: Oxford University Press. 218–39.
- Davies AA, Smith GD, May MT, et al. Association between birth weight and blood pressure is robust, amplifies with age, and may be underestimated. Hypertension (2006) 48:431–6.
[Abstract/Free Full Text] - Victora CG, Barros FC. Commentary: the catch-up dilemma—relevance of Leitch's ‘low-high’ pig to child growth in developing countries. Int J Epidemiol (2001) 30:217–20.
[Free Full Text]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  C. Thomas and C. Power Do early life exposures explain associations in mid-adulthood between workplace factors and risk factors for cardiovascular disease? Int. J. Epidemiol., January 16, 2010; (2010) dyp365v1. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Cournil, A. N. Coly, A. Diallo, and K. B. Simondon Enhanced post-natal growth is associated with elevated blood pressure in young Senegalese adults Int. J. Epidemiol., October 1, 2009; 38(5): 1401 - 1410. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F Mzayek, R Sherwin, J Hughes, S Hassig, S Srinivasan, W Chen, and G S Berenson The association of birth weight with arterial stiffness at mid-adulthood: the Bogalusa Heart Study J Epidemiol Community Health, September 1, 2009; 63(9): 729 - 733. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Sabet, L. M Richter, P. G Ramchandani, A. Stein, M. A Quigley, and S. A Norris Low birthweight and subsequent emotional and behavioural outcomes in 12-year-old children in Soweto, South Africa: findings from Birth to Twenty Int. J. Epidemiol., August 1, 2009; 38(4): 944 - 954. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||